Ontogenetic variation in the crocodylian vestibular system

Abstract

Crocodylians today live in tropical to subtropical environments, occupying mostly shallow waters. Their body size changes drastically during ontogeny, as do their skull dimensions and bite forces, which are associated with changes in prey preferences. Endocranial neurosensory structures have also shown to change ontogenetically, but less is known about the vestibular system of the inner ear. Here we use 30 high-resolution computed tomography (CT) scans and three-dimensional geometric morphometrics to investigate the size and shape changes of crocodylian endosseous labyrinths throughout ontogeny, across four stages (hatchling, juvenile, subadult and adult). We find two major patterns of ontogenetic change. First, the labyrinth increases in size during ontogeny, with negative allometry in relation to skull size. Second, labyrinth shape changes significantly, with hatchlings having shorter semicircular canal radii, with thicker diameters and an overall dorsoventrally shorter labyrinth than those of more mature individuals. We argue that the modification of the labyrinth during crocodylian ontogeny is related to constraints imposed by skull growth, due to fundamental changes in the crocodylian braincase during ontogeny (e.g. verticalisation of the basicranium), rather than changes in locomotion, diet, or other biological functions or behaviours.

Keywords: allometry; crocodylia; morphology; ontogeny; verticalisation; vestibular system.

FIGURE 1

Lateral view of the skull and right endosseous labyrinth of a hatchling specimen of Crocodylus niloticus (NMS Z.1859.13.804). (a) semi‐transparent skull showing the position of the endosseous labyrinth; right endosseous labyrinth in (b) lateral; (c) medial; (d) anterior; (e) posterior; (f) dorsal views. Abbreviations: asc, anterior semicircular canal; cc, crus commune; cd, cochlear duct; lsc, lateral semicircular canal; psc, posterior semicircular canal. Scale bar equals 1 cm

FIGURE 2

Relationship between skull length (mm) and labyrinth length (mm), in crocodylians (log‐transformed) with 95% confidence interval indicating that the labyrinth grows with negative allometry in relation to the skull. Colours and shapes indicate ontogenetic stages; blue/squares, adults; turquoise/rhombus, subadults; orange/triangle, juvenile; magenta/circle, hatchling

FIGURE 3

Principal component analysis (PCA) with morphospace occupation based on ontogenetic stages, showing three distinct clusters, hatchling, juvenile and subadult/adult. (a) PC1 vs. PC2; (b) PC1 vs. PC3. Blue/squares, adults; turquoise/rhombus, subadults; orange/triangle, juvenile; magenta/circle, hatchling

FIGURE 4

Principal component analysis (PCA) with morphospace occupation based on ontogenetic stages for two crocodylian genera for PC1 vs. distinct clusters, hatchling, juvenile and subadult/adult. (a) Alligator; (b) Crocodylidae. Blue/squares, adults; turquoise/rhombus, subadults; orange/triangle, juvenile; magenta/circle, hatchling

FIGURE 5

Ontogenetic variation in the right endosseous labyrinth of Alligator mississippiensis. (a‐e) hatchling (NMS Unreg.); (f‐j) juvenile (UF herp 21461); (k‐o) adult (USNM 211232) in (a,f,k) lateral; (b,g,l) anterior; (c,h,m) posterior; (d,i,n) medial; (e,j,o) dorsal views. Scale bars equal 5 mm

FIGURE 6

Bony labyrinth shape morphospace, separating hatchling, juvenile and subadult/adults specimen based on a canonical variate analysis (CVA) of the PCA scores. Blue/squares, adults; turquoise/rhombus, subadults; orange/triangle, juvenile; magenta/circle, hatchling

FIGURE 7

Lateral (first, third and fifth rows) and dorsal (second, fourth and sixth rows) views of various crocodylian endosseous labyrinths. (a) Osteolaemus tetrapis (FMNH 98936); (b) Gavialis gangeticus (UF‐herp‐118998); (c) Crocodylus acutus (FMNH 59071); (d) Mecistops cataphractus (TMM M‐3529); (e) Crocodylus rhombifer (MNB AB50.0171); (f) Crocodylus moreletti (TMM M‐4980); (g) Crocodylus johnstoni (TMM M‐6807); (h) Caiman crocodylus (FMNH 73711); (i) Gavialis gangeticus (TMM M‐5490); (j) Crocodylus palustris (NMS Z.1968.13.55); (k) Crocodylus porosus (OUVC 10899); (l) Gavialis gangeticus (NMS Unreg.); (m) Melanosuchus niger (NMS Z.1859.13.804); (n) Crocodylus porosus (NMS Z.1925.9.1131); (o) Mecistops sp. (NMS Z.1859.13). (a‐f) adults; (g‐i) subadults; (j‐k) juveniles; (l‐o) hatchlings. Scale bars equal 5 mm

FIGURE 8

Verticalisation of the braincase in Alligator mississippiensis. (a) occipital view, (b) cross‐section of a hatchling specimen (NMS Unreg.); (c) occipital view, (d) cross‐section of an adult specimen (USNM 211232). Abbreviations: an, angular; ar, articular; bo, basioccipital; bs, basisphenoid; ls, laterosphenoid; oc, occipital condyle; ot, otoccipital; pa, parietal; pro, prootic; pt, pterygoid; qua, quadrate; so, supraoccipital; sq, squamosal. Scale bar equals 5 mm in a, b and 10 cm in c, d